Yusuf, L.; Rayner, J. G.; Zhang, R.; Twyman, K.; Paulini, M.; Zhang, X.; Balenger, S. L.; Lee, N.; Tinghitella, R. M.; Gray, D.; Blaxter, M.; Bailey, N. W.

Novel antagonistic interactions between species are expected to drive especially rapid coevolution. However, little is known about the genomic basis of such coevolution in nature because novel inter-specific interactions are rarely observed. Here, we study two species that recently came into first contact in Hawaii, the parasitoid fly Ormia ochracea and its cricket host Teleogryllus oceanicus. The fly locates crickets acoustically using their song, and parasitism usually results in host death. In response, protective male-silencing mutations have rapidly spread through cricket populations over the last ~25 years, imposing novel selective pressure on flies. By integrating population genomic analyses of 358 re-sequenced flies with field surveys of selection imposed by host adaptations, we discover genomic signatures of recent selective sweeps driven by host adaptations, indicative of escalating arms-race dynamics. This evolutionary response is occurring despite severely depleted genetic variation after bottlenecks in Hawaiian fly populations. Comparative analyses suggest that the genomic substrate of modern-day, rapid counter-adaptation in O. ochracea has been under positive selection on intermediate and long-term timescales across parasitoid flies. Our findings thus support predictions of influential arms race coevolution models and illustrate the current and ancient genomic bases of counteradaptation in nature.